Alternative Strategies for Clonal Reproduction 269

Alternative Strategies for Clonal Plant Reproduction©

Robert L. Geneve University of Kentucky, Department of Horticulture, Lexington, Kentucky 40546 U.S.A. Email: [email protected]

INTRODUCTION Pick up any biology textbook and there will be a description of the typical sexual life cycle for . In higher plants, the life cycle starts with seed germination followed by vegetative growth leading to flower and gamete formation with the ultimate goal of creating genetically diverse offspring through seed production. The fern life cycle is more primitive but follows a similar progression from spore germi- nation to the gametophytic generation leading to sexual union of gametes resulting in the leafy sporophyte, which in turn creates the spores. Interestingly, plants have evolved unique alternative life cycles that bypass typi- cal seed production in favor of clonal reproduction systems. This may seem counter- intuitive because sexual reproduction should lead to greater genetic diversity in offspring compared to clonal plants. These sexual offspring should have a higher potential to adapt to new or changing environments, i.e., be more successful. How- ever, investing in clonal reproduction seems to increase the likelihood that a species can colonize specific environmental niches. It has been observed that many of the perennial species in a given ecosystem tend to combine both sexual and clonal forms of reproduction (Ellstrand and Roose, 1987). Additionally, unique clonal propaga- tion systems tend to be more prevalent in plants adapted to extreme environments like arctic, xerophytic, and Mediterranean climates. Mini-Review Objectives. The objective of this mini-review is to describe some of the ways plants have evolved clonal reproduction strategies that allow unique plants to colonize extreme environments.

CLONAL REPRODUCTION ADOPTED BY PLANTS There are two basic forms of clonal reproduction adopted by plants. Flowering plants and ferns can reproduce by modifications of vegetative structures (shoot, leaf, and root). Additionally, flowering plants can produce clonal seeds via apomixis. It is interesting that cycads and gymnosperms that are intermediate in their evolu- tion between ferns and flowering plants do not display alternative clonal propaga- tion strategies. It is possible that morphological adaptations in cycads and gymno- sperms did not permit the plasticity needed for clonal reproduction. Vegetative reproductive systems are incredibly unique, and their diversity is listed in Table 1 and illustrated in Figure 1. These reproductive structures can be aerial or subterranean modifications of stems, leaves, inflorescences, and roots. They range from basal stem modifications that slowly colonize local areas (like off- set production in geophytes) to the production of detachable vegetative plantlets (like aerial bulbils) that can be disseminated much like true seed. Unlike the structural anomalies obvious in vegetative clonal reproduction, there are no obvious outward signs that clones formed through apomixes differ from their sexual counterparts. Apomixis is the production of an embryo that bypasses the usual process of meiosis and fertilization (Hartmann et al., 2002). The genotype 270 Combined Proceedings International Plant Propagators’ Society, Volume 56, 2006

)

)

)

)

Bryophyllum daigremontiana Bryophyllum Camptosorus rhizophyllus Camptosorus Dentaria bulbifera Dentaria (syn. (syn.

woodii (syn. (syn. evansiana stolonifera

(syn. (syn.

C.

subsp.

subsp. (syn. (syn.

Anemone Cornus sericea sericea Cornus Lilium Tulipa Lilium Ceropegia linearis linearis Ceropegia Mimulus gemmiparus Mimulus Solanum tuberosum Solanum Crocus Iris granulata Saxifraga daigremontiana Kalanchoe menziesii Tolmiea bulbiferum Asplenium rhizophyllum Asplenium bulbifera Cystopteris cicutaria Tectaria Fragaria Bambusa Dioscorea alata Dioscorea Begonia grandis grandis Begonia Amorphophallus bulbifer Amorphophallus Cardamine bulbifera Cardamine Liatris

wind flower wind red stem dogwood stem red lily tulip lily rosary vine rosary monkey flower monkey potato crocus iris saxifrage meadow plant piggy-back strawberry thousands of mother bulblet fern bulblet bamboo winged yam winged hardy begonia hardy devil’s tongue devil’s button fern button European bittercress European hen and chick fern chick and hen walking fern walking gayfeather

Bulbs (offsets) Bulbs Rhizomes Tubers (tubercles) tubers Arial Corms (cormels) Corms Stolons (runners) Stolons Arial bulbs (bulbils) (bulbils) bulbs Arial Clonal propagation strategies as alternatives to sexual seed production. seed sexual to alternatives as strategies propagation Clonal

. . . . . c

Modified stems (basal) stems Modified a. b

b

Plantlets on leaves on Plantlets

e

Modified stems (above ground) (above stems Modified a.

d

. . . . 2

Table 1. Table 1

3

Alternative Strategies for Clonal Plant Reproduction 271

Malus Allium vineale Allium Rubus Polygonum viviparum Polygonum helix Hedera Ficus Ficus Neomarica caerulea Neomarica Asimina triloba Asimina americana Agave glomerata Dactylis Pennisetum Poa, Taraxacum Citrus Mangifera Chlorophytum comosum Chlorophytum Poa bulbosa Poa

crabapple wild garlic wild blackberry alpine bistort alpine English ivy English figs dandelion walking iris walking pawpaw plant century grass orchard grasses mango orange spiderplant meadow grass meadow

Gametophytic Sporophytic (adventive embryony) (adventive Sporophytic

. b

Roots on stems on Roots

Plantlets on inflorescence on Plantlets Apomixis a. Plantlets on roots on Plantlets

. . .

5 6. 6. 7

4. 4.

272 Combined Proceedings International Plant Propagators’ Society, Volume 56, 2006

Figure 1. Examples of clonal reproduction systems. (A) Corm and cormel production in gladiola; (B) Aerial bulbils in lily; (C) Aerial tubers in hardy begonia; (D) Plantlets along the leaf margin in mother- of-thousands (Kalanchoe); (E) Aerial bulblets on the frond of bulblet fern; (F) Root suckers in pawpaw; (G) Aerial bulbils in the inflorescence of meadow grass; (H) Multiple apomictic embryos in citrus. of the embryo and resulting plant will be the same as the seed parent. Seed pro- duction via apomixis is clonal. Some species or individuals produce only apomictic embryos; however, the majority of apomictic species produce both apomictic and sexual embryos. Apomixis can be further divided into gametophytic versus sporophytic apomixis. In gametophytic apomixis, the megaspore mother cell fails to initiate or complete meiosis. However, the unreduced (2n) mother cell goes on to form an otherwise nor- mal embryo sac. The egg cell divides to form an embryo but it was never fertilized by a male gamete. The result is clonal seed production. In sporophytic apomixis, the megaspore mother cell does complete meiosis and forms an egg sac with reduced (1n) female gametes. These are fertilized and form normal endosperm and a sexual embryo. However, in addition to this single sexual embryo multiple clonal embryos spontaneously develop from nucellar (2n) tissue surrounding the sexual embryo sac but still inside the developing seed (ovule). The seed usually contains one sexual embryo and multiple asexual embryos. This type of apomixis is a form of polyembryony and is termed adventive embryony. An obvious question for biologists to ponder is whether reliance on vegetative propagation with its inherent reduction in genetic diversity allows the flexibility for a species to adapt to a changing environment and avoid extinction. There are few cases where a species relies on vegetative propagation as its predominant means of propagation. For example, the Minnesota trout lily ( propullans) re- produces by means of a dropper (propagation bulb) produced at the end of a stolon. This general vegetative strategy allows trout lily species to colonize relatively large Alternative Strategies for Clonal Plant Reproduction 273 areas. However, the Minnesota trout lily appears incapable of significant sexual reproduction to supplement vegetative propagation. It only rarely produces seeds and these seeds are thought to be hybrids with white fawnlily (E. albidum) (Banks, 1980). The result is significantly less genetic diversity in Minnesota trout lily com- pared to white fawnlily colonies (Pleasants and Wendel, 1989). Currently, this ge- netic bottleneck leaves the Minnesota trout lily an endangered species found only in two southeastern Minnesota counties. In contrast to the Minnesota trout lily, there are numerous species that repro- duce predominately by vegetative means, but still are capable of seed production. Genetic studies indicate that there is reduced genetic diversity found within local colonies of clonal species and that this diversity increases with geographic distance as the number of dominate clones also increases (Ellstrand and Roose, 1987). The mother plant (genet) can dispense both genetic (seedlings) and clonal progeny (ra- met). When the clonal progeny is very adaptive to a particular environment, it be- comes the dominant reproduction unit (Eriksson, 1997). An extreme example is in aspen (Populus tremuloides) populations that can have over 1000 clonal offspring (ramets) from a single dominant mother plant (genet) covering over 30 acres (Kem- perman and Barnes, 1976). However, even in species where clonal propagation is dominant, sexual progeny from the mother plant provides the genetic flexibility to allow the species to adapt to a changing environment. Sexual reproduction provides essential genetic drift in a species that leads to greater adaptive capacity observed in clonal populations. Some violet species may take the prize for combining the most genetic and clonal strategies for plant reproduction within an individual plant. Violets can produce two types of flowers. Chasmogamous flowers are produced in the spring or summer when pollinators are plentiful and active. Chasmogamous flowers open to permit cross-pollination between flowers and produce offspring (seeds) with generous ge- netic diversity. They also produce subterranean cleistogamous flowers in the au- tumn that never open and self-pollinate. Although this restricts genetic diversity, it does not require the same level of plant resources for seed production and provides insurance against poor seed production from earlier out-crossing flowers. Final- ly, these same violets produce stolons that serve to clonally reproduce successful mother plants. The result is mixed populations of violets that combine two levels of genetically diverse seedling populations and a means for local clonal colonization.

LITERATURE CITED Banks, J.A. 1980. The reproductive biology of Erythronium propullans Gray and sympatric populations of E. albidum Nutt. (). Bull. Torrey Bot. Club 107:181–188. Ellstrand, N.C., and M.L. Roose. 1987. Patterns of genotypic diversity in clonal plant spe- cies. Amer. J. Bot. 74:123–131. Eriksson, O. 1993. Dynamics of genets in clonal plants. Trends Ecol. Evol. 8:313–316. Hartmann, H.T., D.E. Kester, F.T. Davies, Jr., and R.L. Geneve. 2002. Hartmann and Kester’s plant propagation — Principles and practice, 7th ed. Prentice Hall, Upper Saddle River, New Jersey. Kemperman, J.A., and B.V. Barnes. 1976. Clone size in American aspens. Can. J. Bot. 54:2603–2607. Pleasants, J.M., and J.F. Wendel. 1989. Genetic diversity in a clonal narrow endemic, Erythronium propullans, and in its widespread progenitor, . Amer. J. Bot. 76:1136–1151.